A kinetic model of rapidly reversible nonphotochemical quenching

Abstract

Oxygen-evolving photosynthetic organisms possess nonphotochemical quenching (NPQ) pathways that protect against photoinduced damage. The majority of NPQ in plants is regulated on a rapid timescale by changes in the pH of the thylakoid lumen. In order to quantify the rapidly reversible component of NPQ, called qE, we developed a mathematical model of pH-dependent quenching of chlorophyll excitations in Photosystem II. Our expression for qE depends on the protonation of PsbS and the deepoxidation of violaxanthin by violaxanthin deepoxidase. The model is able to simulate the kinetics of qE at low and high light intensities. The simulations suggest that the pH of the lumen, which activates qE, is not itself affected by qE. Our model provides a framework for testing hypothesized qE mechanisms and for assessing the role of qE in improving plant fitness in variable light intensity.regulation of photosynthesis | nonlinear differential equations | biological feedback | chlorophyll fluorescence | photoprotection P hotosynthetic organisms are highly efficient at absorbing photons and transferring energy to a reaction center, where charge separation takes place. However, when the rate of energy consumption by the reaction center is slower than the rate of energy transfer to the reaction center, long-lived chlorophyll excited states build up in the Photosystem II (PSII) antenna. These longlived states present a significant hazard to the organism because the energy contained in excited chlorophyll is sufficient to generate singlet oxygen, which is highly reactive and can break bonds in the proteins essential for photosynthesis (1). Because sufficient light harvesting is necessary for fueling growth, but too much is harmful, plants face a challenge in balancing light harvesting and photoprotection, especially when light intensity rapidly fluctuates between levels that limit photosynthesis and levels that exceed the plant's capacity for photosynthesis (2).The mechanisms of regulated dissipation of excess absorbed energy in the PSII antenna are collectively known as nonphotochemical quenching (NPQ) (3). NPQ mechanisms dissipate excitation energy harmlessly as heat, reducing the extent of photoinhibition (4). There are multiple mechanisms for NPQ and these mechanisms respond on different timescales (3). The most rapid component of NPQ is called qE, and it responds to fluctuations in light intensity on the timescale of seconds to minutes (5, 6).The qE quenching pathway is activated by a decrease in the pH of the thylakoid lumen (3). The low pH of the lumen activates qE by protonating the proteins PsbS (7) and violaxanthin deepoxidase (VDE) (8, 9), and possibly other light harvesting complexes (10, 11). VDE goes on to convert the carotenoid violaxanthin to zeaxanthin in the xanthophyll cycle, which includes the intermediate antheraxanthin (12). The presence of zeaxanthin and the xanthophyll lutein, along with PsbS, is necessary for full expression of qE in vivo. In addition to the protonation of PsbS and the formation of zeaxanthin...

Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes

“…It is also possible that antheraxanthin is involved in the quenching as early antheraxanthin levels were similar across untreated, DTT-treated, and DTSSP-treated thylakoids ( Figure S3b). 37,42 It is noteworthy that a dip in the signal was observed at 5 min in both fluorescence and TA snapshot data. This suggests that the CT quenching is still important in the early stages of NPQ even with reduced VDE activity.…”

Principles of light harvesting from single photosynthetic complexes

“…In addition to the intrinsic conformational heterogeneity and photo-induced conformational dynamics discussed in §3, photosynthetic proteins can also exhibit conformational dynamics in response to changes in the cellular environment caused by fluctuations in light intensity [22]. In particular, these environmentally induced conformational dynamics have been observed and explored in higher plants, and so, in this section, we focus on these type of dynamics in green plants.…”

“…In this way, the environmental conditions control whether PsbS is inactive or active. Thus, the change here is not isolated to a single protein, as discussed in §3, but rather is part of a larger feedback loop within the organism [22]. An area of active investigation is the impact of the environmental conditions associated with high light on the primary antenna complex from green plants, light-harvesting complex II (LHCII).…”

“…Metabolic cost is the energy spent to construct and repair and insert the molecular machinery. Opportunity cost is not capturing energy owing to inoperability or non-optimal functioning of the molecular machinery [22]. Optimizing these two costs guides the principles behind light harvesting under natural conditions.…”

Connection of the Photochemical Reflectance Index (PRI) with the Photosystem II Quantum Yield and Nonphotochemical Quenching Can Be Dependent on Variations of Photosynthetic Parameters among Investigated Plants: A Meta-Analysis

“…However, these photosynthetic parameters can be also affected by other mechanisms. In particular, different components of NPQ can be affected by the pH-dependent protonation of PsbS proteins [37,111], state transition [37,113,114], and photoinhibition [115]. The contribution of these processes to the total NPQ depends on environmental conditions [115,116] and the time of their development [117].…”